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Salmonella Brandenburg in sheep meat in New Zealand


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Salmonella Brandenburg in sheep meat in New Zealand

Mirzet Sabirovic 2002


Salmonella Brandenburg in sheep meat in New Zealand – Preliminary studies to support a risk assessment approach

A Thesis presented in partial fulfillment of the requirements for the degree of Masters of Veterinary Sciences in Veterinary Public Health

At Massey University, Palmerston North, New Zealand

Mirzet Sabirovic



Abortion and death of ewes caused by a particular strain of Salmonella Brandenburg is an animal disease problem that is unique to the South Island of New Zealand. Like most Salmonella serovars, this organism is zoonotic and has caused cases in occupationally exposed people. As Salmonella are primarily recognised as agents of foodborne disease, the potential for foodborne transmission must be acknowledged, although human cases attributed to consumption of sheep meat have not yet been reported. Salmonella Brandenburg has an additional concern for New Zealand’s sheep meat industry owing to the possibility that contamination of sheep meat products could compromise market access. In 1995, the Sanitary Phytosanitary Agreement of the World Trade Organisation specified that scientific risk analysis was required before countries could refuse to import animal or plant materials on the basis of risks to animal, plant, or human health. This thesis presents initial microbiological studies of the prevalence and concentration of Salmonella Brandenburg on sheep meat carcasses that were conducted in conjunction with other projects designed to address the Salmonella Brandenburg issue using a modern risk assessment approach.

The microbiological studies (Chapters 3 and 4) are preceded by two introductory discussions that provide the context for the project. Chapter 1 presents an overview of national and international regulatory approaches to food safety, foodborne diseases and protection of consumer health relevant to meat and meat products. A selective review of literature on Salmonella focuses on Salmonella in sheep and on aspects most relevant to food safety. Chapter 2 summarises information on published quantitative microbiological risk assessments (QRA) conducted using the guidelines developed by the Codex Alimentarius Commission to apply QRA to microbiological foodborne hazards. A conceptual framework is presented for developing a QRA for Salmonella Brandenburg in sheep meat that covers all sectors of the food supply chain from animal production to the point of consumption. Following the precedent of previous QRA efforts, the food supply chain is divided into a series of five modules: animal production; transport and lairage;

slaughter and processing; retail and distribution; and consumer. For each module, key outputs (prevalence and concentration of Salmonella in animals or product at various points in the supply chain), and their likely determinants, are identified. The specific objective of the microbiological studies conducted was to estimate the prevalence and


concentration of Salmonella on sheep carcasses from animals originating from farms that had experienced Salmonella Brandenburg disease and other farms from the same region that had no history of this disease.

Prior to undertaking the field studies, it was necessary to conduct some methodological studies to evaluate the effect of sample handling procedures on the results obtained with quantitative bacteriology. Chapter 3 presents three controlled laboratory experiments with swab samples taken from meat contaminated experimentally with the epidemic strain of Salmonella Brandenburg. The Most Probably Number (MPN) method was used to quantify counts of Salmonella Brandenburg per 100cm2 area of meat swabbed. In each experiment, control samples were processed immediately, and treatment samples were subjected to different periods and conditions of storage. Treatments were chosen to emulate anticipated conditions that would be required for the field studies due to logistic constraints. The three storage protocols evaluated were:

Experiment 1: Storage of swabs diluted in buffered peptone water (BPW) for 48h at 40C Experiment 2: Storage of swabs diluted in BPW for 5 days at 40C

Experiment 3: Storage of swabs for 24h at 40C before dilution in BPW, followed by storage for a further 48h at 40C.

Differences in counts between control and treatment samples were not tested statistically, owing to the small samples sizes, but were numerically less than one log difference in all experiments. In 2 of the 3 experiments, counts for stored samples were in fact numerically greater than for samples processed immediately. These results suggested that carcass swabs contaminated with Salmonella could be stored under the specified conditions without affecting the results of quantitative bacteriology using the MPN method.

Chapter 4 presents a study undertaken to obtain initial qualitative and quantitative estimates of the presence of Salmonella organisms on sheep carcasses sampled at 3 points in the processing chain (i.e. slaughter floor, cooler, and boning room). Slaughtered sheep (ewes and lambs) were sourced from six farms in the Central Otago/Southland region of the South Island where Salmonella Brandenburg disease is endemic. Three farms (case farms) were selected based on the occurrence of an outbreak of Salmonella Brandenburg


disease during the spring of 2000. Three non-case farms from the same region were also sampled. As the disease epidemics are temporally clustered in July and August, well before lambs are sent for slaughter, sampling was replicated after an interval of approximately 2 months to assess likely temporal variation in risk of carcass contamination. For comparative purposes, samples from sheep carcasses were also collected from 6 groups of sheep slaughtered at 2 plants in the North Island where salmonellosis due to Salmonella Brandenburg infection in sheep has not been reported. A total of 1417 carcasses were sampled in the study and initially tested by BAX® test. Of these, 1214 samples were sourced from the 3 case and 3 non-case farms supplying the South Island plant. The remaining 203 carcasses were sampled at the 2 North Island plants. A total of 138 (11.3%) of the 1214 samples collected in the South Island plant tested positive for the presence of Salmonella Brandenburg. No positive findings were obtained from the samples collected in the North Island plants. The vast majority (130 or 94%) of the 138 positive samples was obtained in the first period of sampling, indicating a substantial decline in risk of carcass contamination in the period between the first and second sampling. These findings indicated that the prevalence of carcass contamination with Salmonella Brandenburg was markedly elevated in the region where sheep flocks experienced abortion outbreaks caused by the organism. Although clinical Salmonella Brandenburg enteric disease has not been reported in lambs, the first sampling revealed that overall prevalence of contamination was higher (33%) for lamb carcasses than ewe carcasses (10%) from the same farms. While the prevalence of lamb carcass contamination was comparable for both case and non-case farms, the prevalence of ewe carcass contamination was strongly clustered and only 2 samples were positive from non- case farms. Estimates of the prevalence of contamination were influenced by the location of sampling carcasses (e.g. slaughter floor, cooler), but estimates of bacterial numbers on positive carcasses were generally similar regardless of class of stock, time of sampling, or sampling location in the plant. No positive samples were obtained from swabs of primary cuts in the boning room. Collectively these findings suggest that the emergence of Salmonella Brandenburg infection of sheep in the South Island may have considerable implications for product safety and public health. A strong case can be made for more research to better characterise the potential risks and to explore potential risk mitigation strategies. While the data obtained in this study have provided valuable insights into several important aspects of the issue, due to logistic and other constraints they have


considerable shortcomings with respect to the requirements of the formal QRA. These shortcomings were discussed and evaluated in terms of representativeness and suitability for quantitative risk assessment.

Chapter 5 presents an extension of the conceptual framework for a QRA outlined in Chapter 2, by integrating the data obtained from the bacteriological study, as well as data from other sources. Major data gaps are identified and suggestions are presented with respect to options for ongoing research to advance understanding and management of Salmonella Brandenburg in New Zealand sheep meat. More extensive and representative surveys are required to obtain more reliable data on farm, and within-farm, prevalence of infection as well as more extensive and representative longitudinal studies of the prevalence and concentration of the organism during slaughter and processing. It is considered that more systematic surveys at the time of apparent highest risk would be a more reliable means of assessing potential exposure of consumers than predictive microbiology.



“Never give up, … there is always hope”

This thesis would have not been possible without the co-operation and enthusiasm from the entire Salmonella Brandenburg quantitative risk assessment (QRA) project comprised of professional and dedicated people determined to influence and progress the future. I feel privileged to have had the opportunity to work with this team with the vision and courage to explore the unexplored. I would like to thank the industry (Meat New Zealand) and government (New Zealand Ministry of Agriculture and Food Safety Authority) for providing funding in relation to this thesis.

Special thanks go to my chief supervisor, Professor Peter R. Davies, and my work supervisor Dr Steve Hathaway for their skilful guidance, understanding and patience in broadening my professional perspective, and making this thesis a reality. I found it a rewarding learning experience, challenging, and ultimately successful.

I would like to express my sincere thanks to Guill leRoux, John Mills and the team from AgResearch, Hamilton for their professional approach which highlighted the importance of the teamwork that contributed to parts of this thesis. My sincere appreciation and thanks to Peter van der Logt, Dr Roger Cook, and John Bassett from NZFSA and Gary Clark from LABNET who provided unlimited personal support and professional assistance throughout. I am grateful to Tony Zohrab and the team from NZFSA Animal Products Group for the support provided. I would like to thank people at the Alliance Group Mataura meat plant, particularly Allan Patterson and Jane Marshal who made my field work and stay in the South Island very pleasant and enjoyable.

I would like to thank my mates (David, Glen, Tony, Andrew, Ashley, Richard and Howard) for their friendship and encouragement.

This thesis is dedicated to Heather Fraser and my family for their love, understanding and inspiration to complete this work.


Table of Contents

Abstract... i

Acknowledgements ... v

Table of Contents... vii

List of Figures... xi

List of Tables...xii

List of Abbreviations...xiii

List of Appendices... xiv

Chapter 1: A Review of the Food Safety Environment ... 1

1.1 Introduction ... 1

1.2 Foodborne diseases and pathogens ... 3

1.2.1 Sources ... 3

1.2.2 The role of environment ... 4

1.2.3 Public health... 5 Surveillance ... 5 Economic impact ... 7 Traceability ... 7 Changing consumer habits ... 8 Reactions to foodborne diseases... 9

1.3 Contemporary meat hygiene... 10

1.3.1 Process control ... 12

1.3.2 Hazard Analysis and Critical Control Point (HACCP)... 15 Origins... 15 Issues for consideration ... 17

1.3.3 Risk based approach ... 18 Concept of risk analysis... 18 Risk management framework... 21 World Trade Organisation... 23 Codex and HACCP... 24 Codex and meat hygiene ... 27

1.4 Salmonella – a food safety issue ... 30

1.4.1 General considerations... 31

1.4.2 Diagnosis... 33

1.4.3 Public health... 34 National regulatory actions and international impact ... 35 Swedish Salmonella control programme... 36 United States of America ... 39 New Zealand – Draft policy on detection of Salmonella in meat ... 40

1.4.4 Production/processing industries... 40


1.4.5 Sheep meat and meat products ... 41 New Zealand National Microbiological Database... 42

1.5 Objective of this thesis ...43

Chapter 2: Quantitative microbiological risk assessment – practical application in New Zealand ...45

2.1 Background...45

2.2 Sheep meat as a source of foodborne salmonellosis...46

2.3 Quantitative microbiological risk assessments ...46

2.3.1 Stochastic modelling...48 Exposure assessment in production and slaughter...48 Predictive microbiology ...49 Dose response modelling...50

2.4 Selected QRA models...50

2.4.1 E.coli O157:H7 in ground beef...51

2.4.2 Salmonella in broilers ...53

2.4.3 Listeria monocytogenes in ready-to-eat foods ...55

2.4.4 Salmonella Enteritidis in eggs ...57

2.5 QRA of S. Brandenburg in sheep meat in New Zealand ...58

2.5.1 Outline of pathogen pathway model...61

Chapter 3: Effect of sample storage on detection of Salmonella Brandenburg in swabs of experimentally contaminated meat...66

3.1 Introduction ...66

3.2 Material and Methods...67

3.2.1 Experimental contamination of meat samples ...67

3.2.2 Sample storage treatments ...68

3.2.3 Detection of Salmonella...69 Most Probable Number method ...69

3.3 Results...71

3.3.1 Experiment A ...71

Base MPN ...72


3.3.2 Experiment B ...72


3.3.3 Experiment C ...73

3.4 Discussion ...73

Chapter 4: Prevalence and numbers of Salmonella on sheep and lamb carcasses during processing ...76

4.1 Introduction ...76

4.2 Material and methods ...77

4.2.1 Selection of sheep farms and animals ...77 South Island ...77

(11) North Island ………..78

4.2.2 Sample collection……….79 Preparation ... 79 Sampling of carcasses or primal cuts ... 80 Slaughter floor... 81 Cooling floor (ageing floor)... 83 Boning room... 83 Estimation of the swabbed area of carcasses... 84 Sample handling and transport ... 84

4.2.3 Detection of Salmonella... 84 BAX® PCR detection of S. Brandenburg in field samples (qualitative analysis) ... 84 Culture and DNA extraction ... 84 DNA amplification and detection area ... 85 Reading test results ... 86 Confirmation of BAX® PCR positive samples... 86 Enumeration of Salmonella by MPN (quantitative analysis) ... 87

4.2.3 Analysis of data ... 87

4.3 Results... 88

4.3.1 Summary of overall results... 88

4.3.2 First sampling – (November/December 2000)... 88 BAX® PCR detection of Salmonella (Qualitative results)... 88 Qualitative results by individual farms of origin... 89 Qualitative results by point of sampling during processing ... 90 Enumeration of Salmonella by MPN (quantitative results)... 91

4.3.3 Second sampling – Period B... 94

4.3.4 Discussion ... 94

CHAPTER 5: Analysis of available microbiological data in the context of risk assessment, and identification of future research needs... 101

5.1 Introduction... 101

5.2 Animal production module... 101

5.2.1 Prevalence of infected farms in the region... 103

5.2.2 Within-farm prevalence of S. Brandenburg... 106 Epidemiology of S. Brandenburg infection in sheep ... 107

5.2.3 Future data needs - animal production module... 110

5.3 Transport and lairage module... 110

5.3.1 Future data needs - transport and lairage module ... 112

5.4 Slaughter and processing module ... 112

5.4.1 Sheep slaughter... 113

5.4.2 Slaughter and dressing ... 114

5.4.3 Trimming and washing ... 116

5.4.4 Evisceration/post-mortem inspection... 117

5.4.5 Spray washing ... 117

5.4.6 Cooling floor and chillers... 117


5.4.7 Boning room ... 118

5.4.8 Storage and transportation of the product... 119

5.4.9. Future data needs - slaughter and processing module ...120

5.5 Retail distribution and consumer modules ...120

5.6 Conclusion...121

Appendices ...123

References ...124


List of Figures

Figure 1.1. Potential reactions to foodborne disease……….10

Figure 1.2. Risk management framework steps and activities………...22

Figure 1.3. The new proposed draft Code – Production of fresh meat……….30

Figure 2.1. Influence diagram showing steps in food production process that contribute to level of hazard experienced at the point of consumption………...56

Figure 2.2. A generic exposure assessment model for pathogens in foods………...57

Figure 2.3. Project development for the management of risks associated with Salmonella in sheep………62

Figure 2.4. Description of key model outputs and their likely determinants in respective modules of the pathogen pathway………63

Figure 3.1. Dilution scheme used for MPN method ………70

Figure 3.2. Example of MPN scoring procedure*………71

Figure 4.1. Slaughter floor point of samples collection………80

Figure 4.2. Slaughter floor - first step (sternum/abdomen)………82

Figure 4.3. Slaughter floor - second step (Y-cut)………...82

Figure 4.4. Slaughter floor - second step (forelegs)………...82

Figure 4.5. Slaughter floor - third step (bung area)………82

Figure 4.6. Result of BAX® PCR Salmonella test analysis on electrophoresis gel………...86

Figure 4.7. Total number of Salmonella positive carcasses of lambs or ewes collected on the slaughter floor (SF) or cooling floor (CF) where MPN number was higher than 240 (TNTC), or <240 (low)………93

Figure 5.1: Probability scenario tree for Salmonella Brandenburg infection or fleece contamination of sheep on farms ………102

Figure 5.2. Sheep farms with laboratory confirmed cases of S. Brandenburg infection in affected regions in the South Island (1996 to 2000)………...104

Figure 5.3. Potential routes for regional interfarm spread of S. Brandenburg……….105

Figure 5.4: Flow chart of slaughter plant operations for sheep meat production at Plant A (site of studies reported in Chapter 4)………115


List of Tables

Table 1.1. Principal food sources of the common foodborne pathogens ………...3

Table 1.2. Salmonella: New Zealand Meat Industry Microbiological (Pathogen) Profile, 2001(NMD) ………43

Table 2.1. Farm module: data sources and research initiatives………64

Table 2.2. Processing module: data sources and research initiatives………65

Table 2.3. Storage and distribution module – studies………...65

Table 2.4. Consumer module: data sources and research initiatives………65

Table 3.1. MPN results for samples processed immediately after collection (control) and samples stored for 48hours in BPW solution before processing (treatment)………72

Table 3.2. MPN results for samples processed immediately after collection (control) and samples stored for 5 days in BPW solution before processing (treatment)………72

Table 3.3. MPN results for samples processed immediately after collection (control) and swabs stored 24 hours before dilution in BPW, then a further 48 hours in BPW before processing (treatment)………73

Table 4.1. Sampling dates for ewes and lambs sourced from case (C) and non-case (NC) farms………78

Table 4.2. Proportion of BAX® PCR Salmonella positive carcasses from case and non-case farms at first sampling ……….88

Table 4.3. Proportion of BAX® PCR Salmonella positive lamb and ewe carcasses at first sampling………89

Table 4.4. Proportions of BAX® PCR Salmonella positive carcasses from case farms at first sampling………...89

Table 4.5: Proportions of BAX® PCR Salmonella positive carcasses from non-case farms at first sampling…………...89

Table 4.6. Proportion of BAX® PCR Salmonella positive test samples from lambs from case farms at first sampling ………...90

Table 4.7. Proportion of BAX® PCR Salmonella positive test samples from lambs from non-case farms at first sampling ………...90

Table 4.8. Proportion of BAX® PCR Salmonella positive test samples from ewes from case farms at first sampling ………...91

Table 4.9. Proportion of BAX® PCR Salmonella positive test samples from ewes from non case farms at first sampling ………...91

Table 4.10. Areas (cm2) of sites swabbed on lamb carcasses at first sampling………91

Table 4.11. MPN counts (log10MPN/100cm2) of 34 BAX® PCR Salmonella positive test samples at the first sampling period (MPN number less than < 240)** ………93

Table 4.12. Numbers of Salmonella detected by the MPN method in swabs of 8 BAX® PCR Salmonella positive sheep carcasses at the second sampling………...94


List of Abbreviations

ALOP Appropriate Level Of Protection BSE bovine spongiform encephalopathy CAC Codex Alimentarius Commission CCP Critical Control Point

CCFH Codex Committee on Food Hygiene

ESR The New Zealand Institute of Environmental Sciences & Research Limited

EU European Union

FAO Food and Agriculture Organisation FSO Food Safety Objective

GATT General Agreement on Tariffs and Trade GHP Good Hygiene Practices

GMP Good Manufacturing Practices

HACCP Hazard Analysis and Critical Control Point MPN Most Probable Number method

NMD New Zealand National Microbiological Database NZFSA New Zealand Food Safety Authority

OIE Office International des Epizooties (World Organisation for Animal Health) S. Brandenburg Salmonella enterica subsp. enterica (Brandenburg)

S. Brandenburg - QRA project

Multisectorial quantitative risk assessment project administered by NZFSA and funded primarily by Meat New Zealand over a 3 year period. Sectors include NZFSA, primary producers, the meat processing industry, field veterinarians, Ministry of Health, local health authorities, science providers (Massey University, AgResearch, ESR, LABNET), animal remedy industry SPS Sanitary and Phytosanitary Agreement

QRA Quantitative Risk Assessment VCJD variant Creutzfeldt-Jacob disease

UK United Kingdom

USA United States of America

USDA United States Department of Agriculture USDA-FSIS United States Department of Agriculture

Food Safety and Inspection Services WHO World Health Organisation

WTO World Trade Organisation


List of Appendices

Appendix 1. Reagent Preparation for BAX® test………..………. 124


Chapter 1: A Review of the Food Safety Environment

1.1 Introduction

Humans live in constant interaction with the environment through breathing, drinking and eating. Such an intimate interaction always carries a risk of exposure to harmful pathogens or substances that can affect their health (Roberts et al., 1995a). As a part of the evolutionary process, the long-term trend is interaction between microorganisms and the host (Lederberg, 1998), often resulting in mutually beneficial outcomes.

Animals and animal products comprise an integral part of the socio-economic development and well being of human society. Animals, as a source of food, live in close association with environmental sources of microorganisms, which naturally establish themselves on the hide, hair, hooves, skin, feather, feet, and gastrointestinal tract. Although most of them maybe benign to their animal host and produce no clinical signs of infection or disease, some may have pathogenic effects in another susceptible host, including humans (Buchanan and Halbrook, 1995). The food safety environment related to the consumption of protein derived from animals is complex in nature. Despite various control measures along the entire production chain it is almost impossible to absolutely exclude hazardous pathogens that may pose risks to human health.

Historically meat, poultry, and eggs are considered as a major source of high quality animal protein. Potentially they may harbour, or become environmentally contaminated with certain pathogenic microorganisms during pre-harvest production or processing throughout the food chain (Forsythe, 1996).

Food is a fundamental requirement for survival. Today’s menu of food available for consumption is extensive. In many countries in the world, meat and meat products are high on the list of the most commonly consumed foods. As our ancestors had, modern food producers also consider fresh meat as a highly fragile food product, which unless correctly processed, packaged, stored, and distributed, spoils quickly and becomes hazardous, primarily due to microbial growth.

With increased size and complexity, food production systems have become more vulnerable to a number of potential risk factors. All raw meat can have some level of


microbial contamination present and cannot be expected to be sterile. However, the presence of pathogens in the food supply even in low numbers is undesirable, and within the meat industry, the assurance of meat safety and quality are of paramount importance.

Meat and meat products continue to contribute greatly to New Zealand’s economy (approximately NZ $5.2 bn in export earnings/year). As such, New Zealand is committed to maintain its presence in international markets with products that comply with international requirements and meets high consumer standards. Under the international agreements governed by the World Trade Organisation (WTO), New Zealand is obliged to ensure that existing production systems meet those standards, and have sanitary measures based on sound science and risk assessment techniques.

This thesis addresses a specific microbiological hazard1 in relation to sheep meat food safety and the development of a pathogen/pathway model to assist application of quantitative risk assessment of Salmonella Brandenburg in sheep meat in New Zealand.

The thesis does not consider any other hazards (e.g. chemical hazards and toxins) in meat/meat products. These hazards may be mentioned where relevant.

It was considered appropriate to address multiple aspects relevant to trade in meat and meat products as a foundation for logical flow in addressing the specific research of interest. The 1st Chapter considers regulatory and other issues (e.g. food safety, foodborne diseases and protection of consumer health) relevant to meat and meat products, to provide a general basis for further considerations of the management of the specific risks associated with S. Brandenburg in sheep meat.

1 Hazard refers to a biological agent (i.e. microorganism and/or its toxins) that has the potential to cause an adverse health effect (Lammerding and Fazil, 2000)


1.2 Foodborne diseases and pathogens 1.2.1 Sources

Traditionally, foodborne diseases have been associated with bacteria, and to a lesser extent viruses, fungi and protozoa. Although worldwide data on foodborne diseases occurrence are incomplete, some common trends have started to emerge. While some foodborne pathogens (e.g. Campylobacter) may have the potential to exceed Salmonella in frequency (Buzby, 1995), available information indicates that Salmonella is probably still the most important agent causing acute foodborne disease. S. Enteritidis and S.

Typhimurium are the most commonly implicated serovars, while foods of animal origin, particularly meat and eggs seem to be the most common source (Todd, 1997). While there is a huge number of different microorganisms, until recently it was believed that only a few of them (approximately 20) were agents of foodborne disease in humans (Table 1.1 - adopted from Roberts, 1990):

Table 1.1. Principal food sources of the common foodborne pathogens2

Agent Food Source

Salmonella Raw meat and poultry, eggs

Clostridium perfringens Meats, poultry, dried foods, herbs, spices, vegetable

Staphylococcus aureus Cool foods (much handled during preparation), dairy products, especially if prepared from raw milk

Bacillus cereus and other Bacillus spp. Cereals, dried foods, dry products, meat and meat products, herbs, spices, vegetables

Escherichia coli Many raw foods

Vibrio parahaemoliticus Raw and cooked fish, shellfish, and other seafood

Yersinia enterocolitica Raw meat and poultry, meat products, milk and milk products, vegetables Campylobacter jejuni Raw poultry, meat, raw or inadequately heat-treated milk, untreated water Listeria monocytogenes Meat, poultry, dairy products, vegetables, shellfish

Viruses3 Raw shellfish, cold foods prepared by infected food handlers

* Adopted from Roberts, 1990

During the last decade, improved surveillance of foodborne diseases and new diagnostic techniques resulted in better understanding of foodborne pathogens. It is now considered that more than 200 known diseases are transmitted through food, and that more than half

2(M. Sabirovic - replacement words “foodborne pathogens”)

3 For example, small rounded structured viruses, parvovirus, hepatitis virus


of all recognised cases of foodborne illness have unknown causes (Mead et al., 1999;

Institute of Food Technologists, 2002). It has been realised that some traditional processes are no longer effective in killing some pathogens (e.g. Salmonella in 60-day aged cheese, E. coli O157:H7)(Institute of Food Technologists, 2002). Improved reporting systems indicate significant increases in the incidence of Salmonella, Campylobacter jejuni, enterohaemorrhagic E. coli, and the spread of antibiotic resistant Salmonella Typhimurium DT104 throughout many countries (World Health Organisation, 1999). While some pathogens may cause a great number of illnesses, the case fatality rate may be small and vice versa. On the other hand, the issue is further complicated in cases where a foodborne pathogen (e.g. Listeria monocytogenes, Toxoplasma gondi) may not be harmful to healthy individuals, but may cause severe illness and death in immunocompromised individuals. The emergence of pathogens is a concept that is not well defined or understood by general public. While true emergence could be linked to evolution, the concept of “emergence” may also be linked to better diagnostic techniques leading to public perception of a sudden increase in occurrence of a well-known foodborne pathogen (Institute of Food Technologists, 2002).

1.2.2 The role of environment

The wide distribution of foodborne pathogens in animals and food makes control of foodborne diseases very difficult (Johnston, 1990). Foodborne diseases are complex in nature and often characterised by close interaction between the agent, host and environment (Thrusfield, 1995). The main routes by which foodborne pathogens may reach food may vary from environmental contamination of raw foodstuffs and ingredients to food handling (Roberts, 1990). For example, potential sources of foodborne disease may be indirectly attributed to practices such as using human sewage sludge as fertiliser.

In some cases the source may occur independently of the commercial circuit (e.g. home kill, hunted wild animals), while others may be independent of meat and meat products (e.g. vegetables or fruit) through contaminated irrigation water or biological fertiliser (European Commission, 2000). Besides contaminated foods, live animals on farms, zoos and animal exhibits might be the source of direct zoonotic infection for humans (World Health Organisation, 2001). The emergence of new pathogens and modes of transmission


require better reporting and tracking to obtain a better insight of foodborne diseases, their incidence, severity and economic burden (Buzby, 1995). Therefore, meat and meat products may not always be the source of foodborne infections and disease, as traditionally believed. The issue of potential cross-contamination also requires further investigation to provide a more balanced perspective on other potential primary sources of foodborne diseases, and enable better consumer education. Thus, any potential consumer confusion that may arise because of misunderstanding of perceived food safety issues may be addressed more appropriately.

1.2.3 Public health

Food safety requires the work of industry, government, international partners, producers and consumers. Consumers must also take an active role in preventing foodborne diseases (Liang et al., 2001). In the past it was considered that foodborne diseases mainly occurred because of poor sanitation, hygiene conditions at slaughter, and inadequate refrigeration and canning practices. While food preparation, storage and distribution conditions have improved, new food safety concerns have arisen (Buzby, 1995). During the early 1960s, public concern focused on the use of antibiotics and their residues in meat creating the demand for increased testing for chemicals, residues and toxins in meat. Surveillance

Surveillance for foodborne diseases, usually viewed as a subset of public health surveillance, is one way to identify foodborne disease trends and emergence. In the US, surveillance systems are passive4, active5; national or regional in scope; pathogen- specific6; focused on molecular subtyping schemes (PulseNet)7; or based on a sentinel system of individual sites (FoodNet).8 Traditionally, surveillance was aimed to: (1) identify control and prevent outbreaks, (2) determine the causes, and (3) to monitor trends in occurrence of foodborne diseases. It could also be helpful in defining prevention strategies, and supplying information on the effectiveness of control strategies, a rapid

4 Passive surveillance – Rely on the ability to recognise foodborne diseases or pathogens and willingness to report the diagnosis. Reports voluntarily submitted to appropriate health authorities,

5 Active surveillance – Limited in scope, actively looking for a specific or specified pathogens,

6 e.g. PHLIS (USA) – CDC’s Public Health laboratory Information System for salmonellosis,

7 e.g. PulseNet (USA) – National Molecular Sybtyping Network – takes advantage of molecular biology advances and information technology,


outbreak response, or as a basis for qualitative and quantitative risk assessments (Institute of Food Technologists, 2002). The need for better data has prompted recent establishment of various improved surveillance programmes for foodborne diseases in many other countries, regions or internationally (Institute of Environmental Science &

Research Limited, 2000; Eurosurveillance Weekly, 2000a; Eurosurveillance Weekly, 2000b; World Health Organisation, 2001). Such programmes may provide for more systematic, integrated and co-ordinated data collection, and the on-going recording of data during larger outbreaks. One report (Roberts et al., 1995b) identified that the major problems related to the availability and quality of data on the incidence of foodborne diseases, in particular, uncertainty about their magnitude and distribution, and lack of data linking foodborne disease to specific foods. Although new methods of communication (internet, e-mail groups) make it possible to quickly share data, the report emphasised the need for an integrated approach to the data collection and analysis, and consensus about how these priorities will be set.

As a part of the epidemiological investigation detailed information on the entire food production chain needs to be collected. While it is important to deal immediately with an outbreak, better understanding of foodborne pathogen transmission would significantly help in the assessment of risks and designing appropriate risk management measures to prevent similar events in the future (Tauxe et al., 1997). Meanwhile foodborne diseases still remain one of the most widespread problems in the contemporary world. While improvements are made, the picture generated by surveillance programmes may not be complete. The programmes often do not capture information on small incidents or individual cases where affected consumers may not seek medical help. These occurrences are difficult to estimate.

8 e.g. FoodNet (USA) – Uses active surveillance (public health authorities, clinicians, laboratories),

(25) Economic impact

In 1996, the medical costs and value of lives lost from five types of foodborne infections in England and Wales was estimated at GBP 300-700 million annually. In developing countries (excluding China) the morbidity and mortality associated with diarrhoea was estimated to be in order of 2700 million cases each year, resulting in 2.4 million deaths below the age of five (World Health Organisation, 1999). In New Zealand, the estimated costs of foodborne disease per human case was NZ$ 200 (Scott et al., 2000), while in Sweden the average cost per illness was SEK 2,164 (Lindquist et al., 2001). These figures also illustrate the potential magnitude of the negative impact of foodborne illnesses on health and development. Mead et al., (1999) consider that approximately 76 million foodborne diseases occur in the USA each year, resulting in 325,000 hospitalisations and 5,000 deaths. It is estimated that around 80% of foodborne illnesses were due to unidentified pathogens. Of the cases where a pathogen was identified (38.6 million foodborne diseases) 5.2 million (13%) were due to bacteria, 2.5 million (7%) due to parasites, and 30.9 million (80%) due to viruses (Mead et al., 1999). A comprehensive estimate of the economic costs to individuals (direct and indirect, e.g. lost work and lost household tasks); employers; and food sellers who may experience decreased sales and reputation is lacking. Another component that may need to be factored in is estimating the industry and the public’s willingness to pay for activities aimed at reducing a particular hazard (Kinsey, 1995). Traceability

With global distribution of food, consumers and regulators are demanding stricter safety standards to guarantee safe food delivery. In today’s terms, traceability may be defined as the existence of systems that maintain credible identification of animals or animal products through various steps from “farm to retail”. Identification may originate at any level and at any step of the process in the food chain and should enable both traceback and traceforward. As food production and marketing have been removed from direct consumer control (McKean, 2001), the importance of traceability of animals and animal products has grown significantly.


Many traceability programmes are initiated at national level (e.g. Salmonella programmes in Denmark and Sweden, UK national pork production system, UK response to bovine spongiform encephalopathy (BSE), national brucellosis, tuberculosis, trichinellosis programmes in many countries) or a regional level (e.g. response to bovine spongiform encephalopathy)(McKean, 2001). Apart from increasing standards, retailers have also found that commercial advantage can be gained from certain aspects of source

verification. This led to producer groups developing a multiplicity of assurance schemes9 (Pettitt, 2001) for their own purposes to facilitate dealing with production problems or to increase trade opportunities at the national and international level. Whilst various countries have traceability systems in place, there are no internationally accepted standardised systems (Vallat, 2001) relevant to international trade in both live animals and animal products. Changing consumer habits

Modern life in developed countries is now characterised by rapidly changing eating habits, novel foods, cooking processes (e.g. microwave, irradiation), “fast” foods, health awareness, diets, dining out, and buying food in bulk (Waites and Arbuthnott, 1990). It may be speculated that consumer demand has led to globalisation and centralisation of the food supply and thus has resulted in the dispersal and concentration of pathogens.

Potentially huge numbers of consumers may be exposed to contaminated foodstuffs in a short period of time.

Additionally, the factors most frequently associated with foodborne infections include improper hygiene or handling practices of food handlers and consumers, increased international travel, and increased reliance on imported produce and other food (Doyle et al., 2000). Common sense and knowledge indicate that use of appropriate hygiene, food handling and proper cooking practices may effectively prevent the vast majority of microbial foodborne diseases. The most common observed unhygienic practices (Jay et al., 1999) were infrequent hand washing; inadequate cleaning of kitchen surfaces;

presence of pets in the kitchen; touching the face, mouth, nose, and/or hair during food

9 e.g. National farmers’ Union British Standards scheme, farm quality assurance schemes in many other countries (Pettitt, 2001)


preparation; and lack of separate hand and dish towels. Consumers play a significant role in preventing foodborne diseases by avoiding consumption of undercooked and uncooked high-risk goods, refrigerating perishable foods and disposing of hazardous foods that have been recalled (Liang et al., 2001). Reactions to foodborne diseases

An individual decides what, when and how much to eat. Consumers like to be informed about the risks they are taking when selecting food, and all food suppliers, governments and educators should provide that information (van Schothorst, 1997). Reactions to significant foodborne disease outbreaks, either at the national or international level, are often reflected through increased consumer, legal, and political demands on standards in the trade (Hathaway, 1997). Recent events have led to the implementation of various new regulatory models, focused on science-based standards, and a demand on industry to take a more proactive approach and responsibility for food safety.

The media often quickly picks up “sensational” stories that may cover perceived food safety issues and emergence of new diseases, globalisation and lack of confidence in food production and processing industries, including government and regulators. The most common consumer and regulatory responses associated with foodborne disease outbreaks may be summarised as follows (Figure 1.1)10.

10 Sabirovic M. (August 2002)


Foodborne disease Consumer & regulatory response

Potential significant impact on consumption and market access Create desire to reduce the

risk throughout the food chain from “farm to plate”

Recognition Reporting Information (media) (accurate/inaccurate)

Systematic gathering of data - better epidemiological understanding and objective identification of the possible source of infection

Detailed assessment of risks - selection of appropriate risk management actions

& review in light of the latest scientific information

Figure 1.1. Potential reactions to foodborne disease

Thus, it is considered that there is a clear need for co-operation between food safety professionals and experts in the physio-sociological sector to bring professional insight into the parameters that influence the transmission and assimilation of relevant information. People seemingly accord greater weight to risks imposed by others compared to those they face as a result of personal life choice. The latter are not so readily appreciated but are often more serious risks (Mossel et al., 1998). People are more likely to accept risks if they know the risks and their order of magnitude and have a sense that they may be able to control them. While often people take an additional risk for a particular food they like, in some instances governments have made a decision to restrict the sale of certain products to protect consumers regardless of consumer wants. In many instances, industry may take such action for commercial reasons (e.g. brand image, loss of consumers, liability)(van Schothorst, 1997).

1.3 Contemporary meat hygiene

At the end of the 19th century, the “germ theory” of disease caused control measures (e.g.

meat inspection) to be dictated by a paradigm of disease causation. Meat inspection, quickly adopted by many countries worldwide, originated at a time of poor animal husbandry, prevalent zoonotic diseases (e.g. tuberculosis, brucellosis) and stock presented for slaughter were often old. Meat inspection was primarily focused on detecting and removing diseased animals and any abnormalities from a carcass (Bell, 1993). Regulators


were concerned about all factors affecting hygiene and safety of meat at all stages of production, processing and distribution. This included, animal health and freedom of specified diseases (ante-mortem inspection), safe removal of all contaminated and diseased carcasses or parts thereof (post-mortem inspection), hygiene conditions of all in- plant procedures and proper identification of carcasses and products (Collins, 1995).

Over the past three decades several food safety scares resulted in the rapid decline of public confidence in the role of producers, processors and government in the food supply chain (Pettitt, 2001). Some of the episodes raised the issue of the effectiveness of existing meat inspection practices in detecting the presence of micro-organisms (e.g. Salmonella, Campylobacter, Listeria) on contaminated carcasses (European Commission, 2000). They also highlighted inability of the meat inspection to detect microbial pathogens that do not cause any visible changes to the health of the animal, or the carcass.

Most notably, an outbreak of E. coli O157:H7 in the USA in 1982 (Riley et al., 1983) resulted with severe disease (e.g. heamorrhagic colitis, haemolytic uraemic syndrome, and thrombocytopaenic purpura ) in a number of people (mainly elderly and children).

This outbreak was linked to either the consumption of ground beef sandwiches in restaurants or a fast food chain of restaurants that served undercooked hamburgers.

Another outbreak of E. coli O157:H7 in 1992 resulted in several hundreds of sick people and four child fatalities and prompted North American consumers to began questioning the safety of the food supply (Anonymous, 1994). As a result, public concern and media attention started to shift from residues, particularly pesticides, to microbial contaminants as a greater public health risk (Hueston and Fedorka-Cray, 1995). Huleback and Schlosser (2002) noted that more efficient ways of meat inspection and the establishment of criteria for finished products were recommended to the responsible government agency in 1976. However, the E. coli event in 1990s highlighted the need for a change in traditional meat inspection, and accelerated the introduction of significant changes to the entire USA meat processing industries (Anonymous, 1994).

During the past two decades many important changes have occurred in relation to food control and the development of food standards. Controlling authorities were presented with a number of challenges such as the application of updated scientific methods and risk


assessment, the need for structured decision making processes and the application of these to meat hygiene in order to prevent conflict between regulatory and commercial interests.

Hathaway and McKenzie, (1989) considered that the future food safety and quality systems should be designed on the basis of formal scientifically validated quantitative assessments of actual public health hazards as a prerequisite for any sound modernisation of the existing meat inspection procedures. HACCP, recommended by the WHO since 1985 was considered as a recognised method of risk management for meat production and processing (Edwards et al., 1997).

1.3.1 Process control

Food safety concerns relate to three categories of hazard: physical, chemical and biological. Some physical hazards (e.g. any extraneous objects such as metal, glass, etc) may cause illness or injury to a person consuming the product. Meat inspection procedures are generally effective in detecting and removing physical hazards. However, sampling and testing programmes are required to monitor for the presence of chemical (e.g. dioxin) and microbial hazards (e.g. microbial agents). Some microbial agents (e.g.

bacteria, fungi) may have the ability to multiply on, or in meat. Each group of these hazards, if consumed, may have a major significance for public health. For example, the detection of various bacteria (e.g. E. coli, Salmonella) on the carcass may suggest faecal contamination of meat, primarily during processing. Water, used during processing may be contaminated either with such bacteria or by human viruses of public health concern (e.g. caliciviruses, rotavirus) – hence the requirement to use clean water.

Measures are required to be taken at all points in the farm to plate continuum to include production, transport, slaughter, processing, storage, retail and food preparation (Hogue, et al., 1998) to ensure the microbiological safety of foods. Systematic gathering of reliable testing data related to the occurrence, elimination, prevention and reduction of foodborne pathogens (Kvenberg and Schwalm, 2000) is seen as an essential element for controlling the microbial hazards of concern (Swanson and Anderson, 2000). However, improving the microbiological quality of foods alone is insufficient since food-processing technologies cannot provide absolute assurance of the absence of pathogens. Given that food can be recontaminated, producers are required to adhere strictly to good hygiene measures by following GHP, GMP, and implementation of HACCP along the whole food


chain (Panisello et al., 2000). The main driving force of the HACCP system is continuous evaluation of the hazards (Berends and van Knappen, 1999) where microbiological testing plays an important role in the verification of the effectiveness of the plan.

The emergence of E.coli as a human pathogen of public health concern resulted in the introduction of mandatory microbiological monitoring of meat in the USA. However, it has to be emphasised that, as a part of process control, the meat has been monitored microbiologically in most countries for many years but these programmes were rarely standardised and of no interest to regulators. Containment of microbiological risks is attainable and this goal possibly cannot be achieved by end product testing which is a proven effective strategy when directed towards chemical food safety. Many countries are now developing, or have developed, a range of national standardised programmes to monitor the microbiological status of meat.

Microbiological tests form an integral part of the programme by providing valuable information on critical control points, and trigger actions in the case of non-compliance (Lupien and Kenny, 1998). In the USA, the recently introduced Meat and Poultry Inspection regulations (1996) provide a framework for change (Billy and Wachsmuth, 1997) by improving the safety of meat and poultry products (Schlosser et al., 2000), and establishing pathogen reduction performance standards for Salmonella (Sofos et al., 1999). In addition to the large and medium size establishments (plants), the regulations also apply to very small plants (Mossel et al., 1998). The regulations require countries exporting to the USA, including New Zealand, to adopt the same initiative and embark on the development of microbiological standards within regulatory requirements, and microbiological guidelines to be used by manufacturers or regulators to monitor food manufacturing processes (Harris et al., 1995).

In 1995, the EU Council Decisions 95/409 and 95/411 were designed to regulate the sampling regime and testing for Salmonella. These requirements now apply to all Member States, including exporting countries. The EU Directives 64/433 and 71/118 have also been amended to regulate the requirements for testing of meat for certification purposes (Akewrberg and Brannstorm, 1997). Since 1997, New Zealand has conducted microbiological monitoring of red meat. The programme, currently known as the


National Microbiological Database (NMD) covers all red meat primary processors. It includes testing in approved laboratories with the aim to provide scientifically valid data and enable the definition of cost-effective regulatory microbiological criteria that are qualitatively and quantitatively linked to stated public health goals. Freshly slaughtered carcasses, chilled carcasses, primal cuts (outside-hind legs) and cartons of bulk meat are now tested according to standardised protocols for generic E. coli, aerobic plate count and Salmonella where accumulation of data allows (Hathaway et al., 1999) for:

• development of national performance targets,

• on-going monitoring of national performance and individual premises, and

• provision of scientific data to support design of HACCP plans.

In this respect, USDA-FSIS have recognised New Zealand’s ability to compare performance of individual establishment (premise) by comparing their data with national norms, when discussing the food safety objectives of the United States Pathogen Reduction/HACCP Rule. In light of this, the NMD programme is deemed by the USA as the equivalent to the E. coli testing requirements of the US Rule11. According to the draft policy on the detection of Salmonella in Meat (January 2000), New Zealand “does not accept that testing for Salmonella has any direct value as a control indicator for red meat process in New Zealand for the following reasons: (1) prevalence on carcasses is very low; (2) rare isolations are more likely to reflect farm/transport health status, rather than poor process control; (3) the isolation is more likely to be a chance statistical effect than genuine indicator effect, and (4) the lag time for laboratory analysis means that actions are taken well after the initiating event and their value is really only as a tool for identifying trends, unless there is a specific process failure”. New Zealand advocated that E. coli was a much better process control indicator.

11 Dr Roger L. Cook - Memorandum: New Zealand Meat Hygiene Assurance Programme (17 November 2001), Ministry of Agriculture and Forestry, Food Assurance Authority, PO Box 2526, Wellington


1.3.2 Hazard Analysis and Critical Control Point (HACCP)

Although the food industry bears responsibility for providing safe food for consumption, a framework of laws, regulations and inspection system controls food production.

Modern legislative and regulatory requirements are increasingly focusing on performance based standards, while the methods of achieving specified outcomes is left to producers (Liang et al., 2001). Origins

The Pillsbury Company developed HACCP in 1959 for the USA space programme. The primary objective was to provide astronauts with food free of any harmful substances (e.g. pathogens, toxins, chemicals, physical hazards) that may potentially have had catastrophic consequences for the mission. During the development, questions were raised related to the existing methods of quality control in processing industries to identify foodborne hazards (Bauman, 1995). The HACCP system is a form of process control quality assurance, originally targeted at processed products and limited almost exclusively to the manufacturing environment. The basic principle of the system is to identify potential hazards and faulty practices at an early stage of production. These can then controlled in order to prevent them from constituting risks to consumers or an economic burden on the operator from spoilage or recall of marketed items. This is perceived as the key advantage over other reactive approaches such as inspection and end product testing (“test and hold”) which does not prevent the occurrence of the hazards in the first place (Ehiri et al., 1995). End product testing was seen as inefficient because pathogens occur in small numbers and are not evenly distributed within food. The test and hold procedure system is found to be expensive and resources would be better used if focused on the concept of “prevention” rather than trying to “inspect out” the problem (Harris et al., 1995). As a preventative system of food control HACCP allows for identification of the process flow and points that may contribute to a hazard. These are know as Critical Control Points (CCPs), and are defined as “any point in the chain of food production, from raw materials to finished product, where loss of control could result in unacceptable food safety


risk”(Bauman, 1995). While a competent authority is required to define a critical limit (a criterion) that must be met for each CCP, it is the industry responsibility to develop its own HACCP plan, and ensure that each critical limit controls effectively the identified hazard. In most instances critical limits are industry specific (Manis, 1995).

The first comprehensive HACCP document was published in the USA in 1973 and was used for training (Bauman, 1995). In 1973 the HACCP system was successfully introduced to thermally processed ready-to-eat foods such as low-acid canned products (Buchanan and Whiting, 1998; Huleback and Schlosser, 2002). While many industries were interested in establishing their HACCP plans, broad application of HACCP to the entire USA food industry was not considered until 1985 when an authoritative scientific body concluded that end product testing was not adequate in preventing foodborne diseases. In 1987, the USA Congress required that a programme for fish and seafood certification and inspection that was consistent with the HACCP system be designed (Bauman, 1995). Meat and poultry inspection had changed little in decades and various organisations continue to pressure government to move towards a science-based risk inspection system for meat and poultry. In partial response, the government responded with the development of a new slaughter inspection model that has been tested with volunteer plants as a part of the HACCP-based inspection models project (Cates et al., 2001). In 1992, the HACCP was endorsed by scientific bodies in the USA as an effective and rational means of assuring food safety throughout the food chain (Huleback and Schlosser, 2002).

To protect consumers from foodborne diseases and promote public confidence, the EU (Directive 93/43) and the UK introduced legislation in 1993 that require all food businesses to establish a food control system based on HACCP principles (Powel and Attwell, 1998). The same year, the USA Administration mandated safe handling labels for raw meat and poultry products, and declared the presence of E. coli O157:H7 on raw ground beef as intolerable. A testing program for E. coli was initiated in 1994. The Administration also encouraged the development and use of new technologies in food processing. The Food Safety and Inspection Service (FSIS) of the USDA was asked to design a completely new food safety regulatory system where HACCP supplements, but


not replaces traditional meat inspection with the aim of targeting and reducing harmful bacteria in meat and poultry, and modernising the 90-year-old USDA inspection program (Anonymous, 1998a). The passage of the Pathogen Reduction/Hazard Analysis and Critical Control Point System (HACCP) Rule 1996 (popularly termed “The MegaReg”) introduced radical changes to the regulation and inspection of meat hygiene (Mossel et al., 1998; Hulebak and Schlosser, 2002). The Rule (Anonymous, 1999a):

a) Requires all meat and poultry plants to develop and implement a system of preventive controls, known as HACCP, to improve the safety of their products, b) Sets pathogen reduction performance standards for Salmonella that

slaughterplants and plants producing ground products must meet,

c) Requires all meat and poultry plants to develop and implement written standard operating procedures for sanitation,

d) Requires meat and poultry slaughterplants to conduct microbial testing for generic E. coli to verify the adequacy of their process controls for the prevention of faecal contamination. Issues for consideration

Implementation of HACCP as a risk management tool for food safety has helped standardisation of all significant elements related to production and processing practices.

It has also highlighted a number of other areas that need to be regulated, which potentially adds pressure to finite regulatory resources. This includes significant requirements for verification and compliance, plus requirements for laboratory approval, accreditation and testing. At the same time, there is also a requirement to develop appropriate education material to enable the diverse production and processing systems to be aligned with HACCP principles, while taking into consideration all the differences that exist between the various industries.

Over time, it became apparent that HACCP is based upon information that is limited, often conflicting, and rapidly outdated. HACCP requires a definitive, reliable source of underpinning information on causal agents, ingredients, and contributing factors that is amenable to constant review and updating (Powel and Attwell, 1998). Experience of HACCP implementation has revealed that many regulatory regimes still contain mixed elements of GMP and HACCP (Hathaway S.C – personal communication, 2002). It has


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